Monkeys exhibit human-like gaze biases in economic decisions

  1. Shira M Lupkin
  2. Vincent B McGinty  Is a corresponding author
  1. Rutgers, The State University of New Jersey, United States

Abstract

In economic decision-making individuals choose between items based on their perceived value. For both humans and nonhuman primates, these decisions are often carried out while shifting gaze between the available options. Recent studies in humans suggest that these shifts in gaze actively influence choice, manifesting as a bias in favor of the items that are viewed first, viewed last, or viewed for the overall longest duration in a given trial. This suggests a mechanism that links gaze behavior to the neural computations underlying value-based choices. In order to identify this mechanism, it is first necessary to develop and validate a suitable animal model of this behavior. To this end, we have created a novel value-based choice task for macaque monkeys that captures the essential features of the human paradigms in which gaze biases have been observed. Using this task, we identified gaze biases in the monkeys that were both qualitatively and quantitatively similar to those in humans. In addition, the monkeys' gaze biases were well-explained using a sequential sampling model framework previously used to describe gaze biases in humans-the first time this framework has been used to assess value-based decision mechanisms in nonhuman primates. Together, these findings suggest a common mechanism that can explain gaze-related choice biases across species, and open the way for mechanistic studies to identify the neural origins of this behavior.

Data availability

All data and code used for the analyses and figures included in the present manuscript have been uploaded as an Open Science Framework project (and a linked GitHub account). These files can be accessed at: https://osf.io/hkgmn/

The following data sets were generated
    1. Lupkin SM
    2. McGinty VB
    (2022) NHP-Gaze-Bias
    Open Science Framework: DOI 10.17605/OSF.IO/HKGMN.
The following previously published data sets were used

Article and author information

Author details

  1. Shira M Lupkin

    Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3792-5571
  2. Vincent B McGinty

    Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, United States
    For correspondence
    VINCE.MCGINTY@RUTGERS.EDU
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0883-4301

Funding

Rutgers, The State University of New Jersey (Deans Dissertation Fellowship)

  • Shira M Lupkin

Rutgers, The State University of New Jersey (Academic Advancement Fund)

  • Shira M Lupkin

Rutgers, The State University of New Jersey (Graduate Assistantship through the Behavioral and Neural Sciences Graduate Program)

  • Shira M Lupkin

Whitehall Foundation

  • Vincent B McGinty

Biomedical Research Foundation (Busch Biomedical Research Foundation)

  • Vincent B McGinty

National Institute on Drug Abuse (K01-DA-036659-01)

  • Vincent B McGinty

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures were in accordance with the Guide for the Care and Use of Laboratory Animals (2011)and were approved by the Institutional Animal Care and Use Committees of both Stanford University (APLAC Protocol #9720) and Rutgers University-Newark (PROTO999900861). Surgeries to implant orthopedic head restraints were conducted using full surgical anesthesia using aseptic techniques and instruments, and with analgesics and antibiotics given pre-, intra-, and post-operatively as appropriate.

Copyright

© 2023, Lupkin & McGinty

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 768
    views
  • 110
    downloads
  • 4
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Shira M Lupkin
  2. Vincent B McGinty
(2023)
Monkeys exhibit human-like gaze biases in economic decisions
eLife 12:e78205.
https://doi.org/10.7554/eLife.78205

Share this article

https://doi.org/10.7554/eLife.78205

Further reading

    1. Neuroscience
    Xiaoqian Yan, Sarah Shi Tung ... Kalanit Grill-Spector
    Research Article

    Organizing the continuous stream of visual input into categories like places or faces is important for everyday function and social interactions. However, it is unknown when neural representations of these and other visual categories emerge. Here, we used steady-state evoked potential electroencephalography to measure cortical responses in infants at 3–4 months, 4–6 months, 6–8 months, and 12–15 months, when they viewed controlled, gray-level images of faces, limbs, corridors, characters, and cars. We found that distinct responses to these categories emerge at different ages. Reliable brain responses to faces emerge first, at 4–6 months, followed by limbs and places around 6–8 months. Between 6 and 15 months response patterns become more distinct, such that a classifier can decode what an infant is looking at from their brain responses. These findings have important implications for assessing typical and atypical cortical development as they not only suggest that category representations are learned, but also that representations of categories that may have innate substrates emerge at different times during infancy.

    1. Neuroscience
    2. Stem Cells and Regenerative Medicine
    Desiree Böck, Maria Wilhelm ... Gerald Schwank
    Research Article

    Parkinson’s disease (PD) is a multifactorial disease caused by irreversible progressive loss of dopaminergic neurons (DANs). Recent studies have reported the successful conversion of astrocytes into DANs by repressing polypyrimidine tract binding protein 1 (PTBP1), which led to the rescue of motor symptoms in a chemically-induced mouse model of PD. However, follow-up studies have questioned the validity of this astrocyte-to-DAN conversion model. Here, we devised an adenine base editing strategy to downregulate PTBP1 in astrocytes and neurons in a chemically-induced PD mouse model. While PTBP1 downregulation in astrocytes had no effect, PTBP1 downregulation in neurons of the striatum resulted in the expression of the DAN marker tyrosine hydroxylase (TH) in non-dividing neurons, which was associated with an increase in striatal dopamine concentrations and a rescue of forelimb akinesia and spontaneous rotations. Phenotypic analysis using multiplexed iterative immunofluorescence imaging further revealed that most of these TH-positive cells co-expressed the dopaminergic marker DAT and the pan-neuronal marker NEUN, with the majority of these triple-positive cells being classified as mature GABAergic neurons. Additional research is needed to fully elucidate the molecular mechanisms underlying the expression of the observed markers and understand how the formation of these cells contributes to the rescue of spontaneous motor behaviors. Nevertheless, our findings support a model where downregulation of neuronal, but not astrocytic, PTBP1 can mitigate symptoms in PD mice.